High-gamma modulation language mapping and cognitive outcomes after epilepsy surgery.
electrical stimulation mapping
epilepsy surgery
functional brain mapping
stereo‐EEG
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
20 Aug 2024
20 Aug 2024
Historique:
revised:
31
07
2024
received:
24
05
2024
accepted:
01
08
2024
medline:
20
8
2024
pubmed:
20
8
2024
entrez:
20
8
2024
Statut:
aheadofprint
Résumé
We evaluated changes in cognitive domains after neurosurgical lesioning of cortical sites with significant high-gamma power modulations (HGM) during a visual naming task, although these sites were found language-negative on standard-of-care electrical stimulation mapping (ESM). In drug-resistant epilepsy patients who underwent resection/ablation after stereo-electroencephalography (SEEG), we computed reliable change indices (RCIs) from a battery of presurgical and 1-year postsurgical neuropsychological assessments. We modeled RCIs as a function of lesioning even one HGM language site, number of HGM language sites lesioned, and the magnitude of naming-related HGM. The analyses were adjusted for 1-year seizure freedom, operated hemispheres, and the volumes of surgical lesions. In 37 patients with 4455 SEEG electrode contacts (1839 and 2616 contacts in right and left hemispheres, respectively), no ESM language sites were lesioned. Patients with lesioning of even one HGM language site showed significantly lower RCIs for Peabody Picture Vocabulary Test (PPVT), working memory, and verbal learning immediate (VLI) scores. RCI declines with higher number of HGM language sites lesioned were seen in PPVT (slope [β] = -.10), working memory (β = -.10), VLI (β = -.14), and letter-word identification (LWI; β = -.14). No neuropsychological domains improved after lesioning of HGM language sites. Significant effects of the HGM magnitude at lesioned sites were seen on working memory (β = -.31), story memory immediate (β = -.27), verbal learning recognition (β = -.18), LWI (β = -.16), spelling (β = -.49), and passage comprehension (β = -.33). Because working memory was significantly affected in all three analyses, patients with maximal working memory decline were examined post hoc, revealing that all such patients had HGM naming sites lesioned in the posterior quadrants of either hemisphere. HGM language mapping should be used as an adjunct to ESM in clinical practice and may help counsel patients/families about postsurgical cognitive deficits.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIH HHS
ID : R01 NS115929
Pays : United States
Informations de copyright
© 2024 International League Against Epilepsy.
Références
Hermann BP, Perrine K, Chelune GJ, Barr W, Loring DW, Strauss E, et al. Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches. Neuropsychology. 1999;13:3–9.
Sakpichaisakul K, Byars AW, Horn PS, Aungaroon G, Greiner HM, Mangano FT, et al. Neuropsychological outcomes after pediatric epilepsy surgery: role of electrical stimulation language mapping. Seizure. 2020;25(80):183–191.
Arya R, Horn PS, Crone NE. ECoG high‐gamma modulation versus electrical stimulation for presurgical language mapping. Epilepsy Behav. 2017;13(79):26–33.
Kojima K, Brown EC, Matsuzaki N, Rothermel R, Fuerst D, Shah A, et al. Gamma activity modulated by picture and auditory naming tasks: intracranial recording in patients with focal epilepsy. Clin Neurophysiol. 2013;124:1737–1744.
Arya R, Roth C, Leach JL, Middeler D, Wilson JA, Vannest J, et al. Neuropsychological outcomes after resection of cortical sites with visual naming associated electrocorticographic high‐gamma modulation. Epilepsy Res. 2019;29(151):17–23.
Sonoda M, Rothermel R, Carlson A, Jeong JW, Lee MH, Hayashi T, et al. Naming‐related spectral responses predict neuropsychological outcome after epilepsy surgery. Brain. 2022;18(145):517–530.
Hickok G. The functional neuroanatomy of language. Phys Life Rev. 2009;6:121–143.
Hickok G, Poeppel D. Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition. 2004;92:67–99.
Duffau H, Moritz‐Gasser S, Mandonnet E. A re‐examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang. 2014;131:1–10.
Ervin B, Buroker J, Byars AW, Rozhkov L, Leach JL, Horn PS, et al. A distributed network supports spatiotemporal cerebral dynamics of visual naming. Clin Neurophysiol. 2021;132:2948–2958.
Arya R, Ervin B, Dudley J, Buroker J, Rozhkov L, Scholle C, et al. Electrical stimulation mapping of language with stereo‐EEG. Epilepsy Behav. 2019;15(99):106395.
Arya R, Ervin B, Holloway T, Dudley J, Horn PS, Buroker J, et al. Electrical stimulation sensorimotor mapping with stereo‐EEG. Clin Neurophysiol. 2020;131:1691–1701.
Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn. 1980;6:174–215.
Ervin B, Buroker J, Rozhkov L, Holloway T, Horn PS, Scholle C, et al. High‐gamma modulation language mapping with stereo‐EEG: a novel analytic approach and diagnostic validation. Clin Neurophysiol. 2020;131:2851–2860.
Duff K. Evidence‐based indicators of neuropsychological change in the individual patient: relevant concepts and methods. Arch Clin Neuropsychol. 2012;27:248–261.
Busch RM, Lineweaver TT, Ferguson L, Haut JS. Reliable change indices and standardized regression‐based change score norms for evaluating neuropsychological change in children with epilepsy. Epilepsy Behav. 2015;47:45–54.
Goodglass H, Kaplan E, Weintraub S. Boston naming test record. Booklet: Lippincott Williams & Wilkins; 2001.
Mitrushina M, Boone KB, Razani J, D'Elia LF. Handbook of normative data for neuropsychological assessment. New York, NY: Oxford University Press; 2005.
Sherman EM, Wiebe S, Fay‐McClymont TB, Tellez‐Zenteno J, Metcalfe A, Hernandez‐Ronquillo L, et al. Neuropsychological outcomes after epilepsy surgery: systematic review and pooled estimates. Epilepsia. 2011;52:857–869.
European Federation of Neurological Societies Task Force. Pre‐surgical evaluation for epilepsy surgery ‐ European standards. Eur J Neurol. 2000;7:119–122.
Jayakar P, Gaillard WD, Tripathi M, Libenson MH, Mathern GW, Cross JH, et al. Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia. 2014;55:507–518.
Ives‐Deliperi VL, Butler JT. Naming outcomes of anterior temporal lobectomy in epilepsy patients: a systematic review of the literature. Epilepsy Behav. 2012;24:194–198.
Arya R, Frink C, Kargol C, Byars AW, Huddleston D, Diedenhofer DB, et al. Neuropsychological outcomes after epilepsy surgery: a comparison of stereo‐EEG and subdural electrodes. Eur J Neurol. 2023;30:2986–2998.
Hamberger MJ. Cortical language mapping in epilepsy: a critical review. Neuropsychol Rev. 2007;17:477–489.
Wellmer J, Weber C, Mende M, von der Groeben F, Urbach H, Clusmann H, et al. Multitask electrical stimulation for cortical language mapping: hints for necessity and economic mode of application. Epilepsia. 2009;50:2267–2275.
Hamberger MJ, Goodman RR, Perrine K, Tamny T. Anatomic dissociation of auditory and visual naming in the lateral temporal cortex. Neurology. 2001;9(56):56–61.
Hamberger MJ, Seidel WT, McKhann GM 2nd, Perrine K, Goodman RR. Brain stimulation reveals critical auditory naming cortex. Brain. 2005;128:2742–2749.
Prueckl R, Kapeller C, Potes C, Korostenskaja M, Schalk G, Lee KH, et al. CortiQ ‐ clinical software for electrocorticographic real‐time functional mapping of the eloquent cortex conference proceedings. Annual international conference of the IEEE engineering in medicine and biology society IEEE engineering in medicine and biology society conference. New York, NY: IEEE (Institute of Electrical and Electronics Engineers). Volume 2013; 2013. p. 6365–6368.
Milsap G, Collard M, Coogan C, Crone NE. BCI2000Web and WebFM: browser‐based tools for brain computer interfaces and functional brain mapping. Front Neurosci. 2019;12:1–10. Technology Report.
Baddeley A. Working memory ‐ the Interface between memory and cognition. J Cogn Neurosci. 1992;4:281–288.
Muller NG, Knight RT. The functional neuroanatomy of working memory: contributions of human brain lesion studies. Neuroscience. 2006;139:51–58.
Wilson SJ, Baxendale S, Barr W, Hamed S, Langfitt J, Samson S, et al. Indications and expectations for neuropsychological assessment in routine epilepsy care: report of the ILAE neuropsychology task force, diagnostic methods commission, 2013‐2017. Epilepsia. 2015;56:674–681.
Lee GP. Neuropsychology AAoC. Neuropsychology of Epilepsy and Epilepsy Surgery: Oxford University Press, USA; 2010.
Linden DEJ. The working memory networks of the human brain. Neuroscientist. 2007;13:257–267.
Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8:393–402.
Nakai Y, Sugiura A, Brown EC, Sonoda M, Jeong JW, Rothermel R, et al. Four‐dimensional functional cortical maps of visual and auditory language: intracranial recording. Epilepsia. 2019;60:255–267.
Nakai Y, Jeong JW, Brown EC, Rothermel R, Kojima K, Kambara T, et al. Three‐ and four‐dimensional mapping of speech and language in patients with epilepsy. Brain. 2017;1(140):1351–1370.
Strauss E, Sherman EMS, Spreen O. A compendium of neuropsychological tests: administration, norms, and commentary. 3rd ed. New York, NY: Oxford University Press; 2006.
Baxendale S, Wilson SJ, Baker GA, Barr W, Helmstaedter C, Hermann BP, et al. Indications and expectations for neuropsychological assessment in epilepsy surgery in children and adults. Epileptic Disord. 2019;1(21):221–234.
Arya R, Wilson JA, Fujiwara H, Vannest J, Byars AW, Rozhkov L, et al. Electrocorticographic high‐gamma modulation with passive listening paradigm for pediatric extraoperative language mapping. Epilepsia. 2018;59:792–801.
Ueda R, Sakakura K, Mitsuhashi T, Sonoda M, Firestone E, Kuroda N, et al. Cortical and white matter substrates supporting visuospatial working memory. Clin Neurophysiol. 2024;162:9–27.